Exogenous salicylic acid positively affects morpho-physiological and molecular responses of Impatiens walleriana plants grown under drought stress

Abstract

The aim of this experiment was to investigate the exogenous application of salicylic acid (SA) on morpho-physiological and molecular characteristics of Impatiens walleriana plants grown under water deficit stress. Three levels of soil water contents (95, 85, and 75% of field capacity; FC) and three levels of SA (0, 1, and 2 mM) were applied on two impatient cultivars (‘Tempo’ and ‘Salmon’). The results showed that increasing water deficit stress negatively affected growth and flowering characteristics. On the contrary, the foliar application of SA reduced the adverse effect of water deficit stress and improved growth and ornamental plant attributes. Water deficit increased the amount of electrolyte leakage (EL), malondialdehyde (MDA), peroxidase (POD) and ascorbate peroxidase (APX) activities; and proline content. The expression of the gene encoding for Δ1-pyrroline-5-carboxylate synthetase (P5CS) was slightly increased under control treatment (95% FC + SA 0 mM) and then significantly increased at 75% FC and after the SA treatments. The expression pattern of P5CR (Δ1-pyrroline-5-carboxylate reductase gene) was similar to that of P5CS, with differences in terms of intensity. The application of SA reduced the amount of EL and MDA through increased antioxidant activities and water balance. Overall, the results of this study showed that ‘Salmon’ cultivar was able to tolerate drought stress conditions better than ‘Tempo.’ The application of 2 mM SA increased growth and physiological indices in drought-stressed impatient, mitigating the detrimental effects of water deficit in this important ornamental species.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Abassi NA, Kushad MM, Endress AG (1998) Active oxygen-scavenging enzymes activities in developing apple flowers and fruits. Sci Hort 74(3):183–194. https://doi.org/10.1016/S0304-4238(98)00077-6

    Article  Google Scholar 

  2. Alam MM, Hasanuzzaman M, Nahar K, Fujita M (2013) Exogenous salicylic acid ameliorates short-term drought stress in mustard (Brassica juncea L.) seedlings by up-regulating the antioxidant defense and glyoxalase system. Aust J Crop Sci 7(7):1053

    CAS  Google Scholar 

  3. Ananieva EA, Christova KN, Popova LP (2004) Exogenous treatment with salicylic acid leads to increased antioxidant capacity in leaves of barley plants exposed to Paraquat. J Plant Physiol 161:319–328. https://doi.org/10.1078/0176-1617-01022

    CAS  Article  Google Scholar 

  4. Anjum NA, Lopez-Lauri F (2011) Plant Nutrition and Abiotic Stress Tolerance III. Global Science Books, Ikenobe

    Google Scholar 

  5. Antonić S, Milošević A, Cingel M, Lojić M, Trifunović-Momčilov M, Petrić A, Subotić A, Simonović A (2016) Effects of exogenous salicylic acid on Impatiens walleriana L. grown in vitro under polyethylene glycol-imposed drought. South Afr J Bot 105:226–233. https://doi.org/10.1016/j.sajb.2016.04.002

    CAS  Article  Google Scholar 

  6. Armengaud P, Thiery L, Buhot N, Grenier-DeMarch G, Savouré A (2004) Transcriptional regulation of proline biosynthesis in Medicago truncatula reveals developmental and environmental specific features. Physiol Plant 120(3):442–450. https://doi.org/10.1111/j.0031-9317.2004.00251.x

    CAS  Article  Google Scholar 

  7. Bajji M, Lutts S, Kinet JM (2000) Physiological changes after exposure to and recovery from polyethylene glycol-induced water deficit in roots and leaves of durum wheat (Triticum durum Desf.) cultivars differing in drought resistance. J Plant Physiol 157:100–108. https://doi.org/10.1016/S0176-1617(00)80142-X

    CAS  Article  Google Scholar 

  8. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207

    CAS  Article  Google Scholar 

  9. Bidabadi SS, Mahmood M, Baninasab B, Ghobadi C (2012) Influence of salicylic acid on morphological and physiological responses of banana (Musa acuminate cv. Berangan, AAA) shot tips to in vitro water stress induced by polyethylene glycol. Plant Omics J 5:33–39

    CAS  Google Scholar 

  10. Blanusa T, Vysini E, Cameron RW (2009) Growth and flowering of Petunia and Impatiens: effects of competition and reduced water content within a container. HortScience 44(5):1302–1307. https://doi.org/10.21273/HORTSCI.44.5.1302

    Article  Google Scholar 

  11. Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Meth Enzymol 52:302–310. https://doi.org/10.1016/s0076-6879(78)52032-6

    CAS  Article  Google Scholar 

  12. Chen Z, Iyer S, Caplan A, Klessig DF, Fan B (1997) Differential accumulation of salicylic acid and salicylic acid-sensitive catalase in different rice tissues. Plant Physiol 114:193–201. https://doi.org/10.1104/pp.114.1.193

    CAS  Article  Google Scholar 

  13. Costa M, Civell PM, Chaves AR, Martinez GA (2005) Effects of ethephon and 6- benzylaminopurine on chlorophyll degrading enzymes and peroxidase-linked chlorophyll bleaching during post-harvest senescence of broccoli (Brassica oleracea L.) at 20°C. Postharvest Biol Technol 35:191–199. https://doi.org/10.1016/j.postharvbio.2004.07.007

    CAS  Article  Google Scholar 

  14. Damalas CA (2019) Improving drought tolerance in sweet basil (Ocimum basilicum) with salicylic acid. Sci Hort 246:360–365. https://doi.org/10.1016/j.scienta.2018.11.005

    CAS  Article  Google Scholar 

  15. Demiralay M, Sağlam A, Kadioğlu A (2013) Salicylic acid delays leaf rolling by inducing antioxidant enzymes and modulating osmoprotectant content in Ctenanthe setosa under osmotic stress. Turk J Bio 37:49–59

    CAS  Google Scholar 

  16. Dobriyal P, Qureshi A, Badola R, Hussain SA (2012) A review of the methods available for estimating soil moisture and its implications for water resource management. J Hydrol 458:110–117. https://doi.org/10.1016/j.jhydrol.2012.06.021

    Article  Google Scholar 

  17. Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. In: Lichtfouse E, Navarrete M, Debaeke P, Véronique S, Alberola C (eds) Sustainable agriculture. Springer, Dordrecht, pp 153–188

    Google Scholar 

  18. Hayat Q, Hayat S, Irfan M, Ahmad A (2010) Effect of exogenous salicylic acid under changing environment: a review. Environ Exp Bot 68:14–25. https://doi.org/10.1016/j.envexpbot.2009.08.005

    CAS  Article  Google Scholar 

  19. Hayat S, Hasan SA, Fariduddin Q, Ahmad A (2008) Growth of tomato (Lycopersicon esculentum) in response to salicylic acid under water stress. J Plant Interact 3:297–304. https://doi.org/10.1080/17429140802320797

    CAS  Article  Google Scholar 

  20. Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466. https://doi.org/10.4161/psb.21949

    CAS  Article  Google Scholar 

  21. Horvath E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26:290–300. https://doi.org/10.1007/s00344-007-9017-4

    CAS  Article  Google Scholar 

  22. Hu CA, Delauney A, Verma DS (1992) A bifunctional enzyme (delta1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proc Natl Acad Sci USA 89:9354–9358. https://doi.org/10.1073/pnas.89.19.9354

    CAS  Article  Google Scholar 

  23. Huo Y, Wang M, Wei Y, Xia Z (2016) Overexpression of the maize psbA gene enhances drought tolerance through regulating antioxidant system, photosynthetic capability, and stress defense gene expression in tobacco. Front Plant Sci 6:1223. https://doi.org/10.3389/fpls.2015.01223

    Article  Google Scholar 

  24. Idrees M, Masroor M, Khan A, Aftab T, Naeem M, Hashmi N (2010) Salicylic acid-induced physiological and biochemical changes in lemongrass varieties under water stress. J Plant Interact 5:293–303. https://doi.org/10.1080/17429145.2010.508566

    CAS  Article  Google Scholar 

  25. Kadioglu A, Saruhan N, Sağlam A, Terz R, Acet T (2011) Exogenous salicylic acid alleviates effects of long term drought stress and delays leaf rolling by inducing antioxidant system. Plant Growth Regul 64:27–37. https://doi.org/10.1007/s10725-010-9532-3

    CAS  Article  Google Scholar 

  26. Khan MIR, Fatma M, Per TS, Anjum NA, Khan NA (2015) Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front Plant Sci 6:1–17. https://doi.org/10.3389/fpls.2015.00462

    Article  Google Scholar 

  27. Khan MIR, Iqbal N, Masood A, Per TS, Khan NA (2013) Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signal Behav 8(11):e26374. https://doi.org/10.4161/psb.26374

    CAS  Article  Google Scholar 

  28. Kukreja S, Nandval AS, Kumar N, Sharma SK, Sharma SK, Unvi V, Sharma PK (2005) Plant water status, H2O2 scavenging enzymes, ethylene evolution and membrane integrity of Cicer arietinum roots as affected by salinity. Biol Plant 49:305–308. https://doi.org/10.1007/s10535-005-5308-4

    CAS  Article  Google Scholar 

  29. La VH, Lee BR, Islam MT, Park SH, Jung HI, Bae DW, Kim TH (2019a) Characterization of salicylic acid-mediated modulation of the drought stress responses: reactive oxygen species, proline, and redox state in Brassica napus. Environ Exp Bot 157:1–10. https://doi.org/10.1016/j.envexpbot.2018.09.013

    CAS  Article  Google Scholar 

  30. La VH, Lee BR, Zhang Q, Park SH, Islam MT, Kim TH (2019b) Salicylic acid improves drought-stress tolerance by regulating the redox status and proline metabolism in Brassica rapa. Hortic Environ Biotechnol 60(1):31–40. https://doi.org/10.1007/s13580-018-0099-7

    CAS  Article  Google Scholar 

  31. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Meth Enzymol 148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1

    CAS  Article  Google Scholar 

  32. Lipiec J, Doussan C, Nosalewicz A, Kondracka K (2013) Effect of drought and heat stresses on plant growth and yield: a review. Int Agrophys 27(4):463–547. https://doi.org/10.2478/intag-2013-0017

    Article  Google Scholar 

  33. Liu CC, Liu YG, Guo K, Fan DY, Li GG, Zheng YR, Yu LF, Yang R (2011) Effect of drought on pigments, osmotic adjustment and antioxidant enzymes in six woody plant species in karst habitats of southwestern China. Environ Exp Bot 71:174–183. https://doi.org/10.1016/j.envexpbot.2010.11.012

    CAS  Article  Google Scholar 

  34. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262

    CAS  Article  Google Scholar 

  35. MacAdam JW, Nelson CJ, Sharp RE (1992) Peroxidase activity in the leaf elongation zone of tall fescue: I. Spatial distribution of ionically bound peroxidase activity in genotypes differing in length of the elongation zone. Plant Physiol 99(3):872–878. https://doi.org/10.1104/pp.99.3.872

    CAS  Article  Google Scholar 

  36. Maghsoudi K, Emam Y, Ashraf M, Arvin MJ (2019) Alleviation of field water stress in wheat cultivars by using silicon and salicylic acid applied separately or in combination. Crop Pasture Sci 70(1):36–43. https://doi.org/10.1071/CP18213

    CAS  Article  Google Scholar 

  37. Marcińska I, Czyczyło-Mysza I, Skrzypek E, Grzesiak MT, Janowiak F, Filek M, Dziurka M, Dziurka K, Waligórski P, Juzoń K, Cyganek K, Grzesiak S (2013) Alleviation of osmotic stress effects by exogenous application of salicylic or abscisic acid on wheat seedlings. Int J Mol Sci 14:13171–13193. https://doi.org/10.3390/ijms140713171

    CAS  Article  Google Scholar 

  38. Misra N, Saxena P (2009) Effect of salicylic acid on proline metabolism in lentil grown under salinity stress. Plant Sci 177:181–189. https://doi.org/10.1016/j.plantsci.2009.05.007

    CAS  Article  Google Scholar 

  39. Miura K, Tada Y (2014) Regulation of water, salinity, and cold stress responses by salicylic acid. Front Plant Sci 5:4. https://doi.org/10.3389/fpls.2014.00004

    Article  Google Scholar 

  40. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232

    CAS  Article  Google Scholar 

  41. Nazar R, Umar S, Khan NA, Sareer O (2015) Salicylic acid supplementation improves photosynthesis and growth in mustard through changes in proline accumulation and ethylene formation under drought stress. S Afr J Bot 98:84–94. https://doi.org/10.1016/j.sajb.2015.02.005

    CAS  Article  Google Scholar 

  42. Nazarli H, Zardashti MR, Darvishzadeh R, Najafi S (2010) The effect of water stress and polymer on water use efficiency, yield and several morphological traits of sunflower under greenhouse condition. Not Sci Biol 2(4):53–58

    Article  Google Scholar 

  43. Odjegba VJ, Adeniyi AM (2012) Responses of Celosia argentea L. to simulated drought and exogenous salicylic acid. Nat Sci 10:252–258

    Google Scholar 

  44. Okuma E, Nozawa R, Murata Y, Miura K (2014) Accumulation of endogenous salicylic acid confers drought tolerance to Arabidopsis. Plant Signal Behav. https://doi.org/10.4161/psb.28085

    Article  Google Scholar 

  45. Roosens NH, Thu TT, Iskandar HM, Jacobs M (1998) Isolation of ornithine-d-amino transferase cDNA and effect of salt stress on its expression in Arabidopsis thaliana. Plant Physiol 117:263–271. https://doi.org/10.1104/pp.117.1.263

    CAS  Article  Google Scholar 

  46. Shi Q, Bao Z, Zhu Z, Ying Q, Qian Q (2006) Effects of different treatments of salicylic acid on heat tolerance, chlorophyll fluorescence, and antioxidant enzyme activity in seedlings of Cucumis sativa L. Plant Growth Regul 48:127–135. https://doi.org/10.1007/s10725-005-5482-6

    CAS  Article  Google Scholar 

  47. Singh B, Usha K (2003) Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress. Plant Growth Regul 39:137–141. https://doi.org/10.1023/A:1022556103536

    CAS  Article  Google Scholar 

  48. Sokal RR, Rohlf FJ (1997) Biometry: the principles and practice of statistic in biological research. WH Freeman, New York

    Google Scholar 

  49. Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15(2):89–97. https://doi.org/10.1016/j.tplants.2009.11.009

    CAS  Article  Google Scholar 

  50. Tavakoli M, Poustini K, Alizadeh H (2016) Proline accumulation and related genes in wheat leaves under salinity stress. J Agr Sci Tech 18:707–716

    Google Scholar 

  51. Verbruggen N, Hermans C (2008) Pro accumulation in plants: a review. Amino Acids 35:753–759. https://doi.org/10.1007/s00726-008-0061-6

    CAS  Article  Google Scholar 

  52. Verslues PE, Sharma S (2010) Proline metabolism and its implications for plant- environment interaction. Arabidopsis Book 8:344–342. https://doi.org/10.1199/tab.0140

    Article  Google Scholar 

  53. Wang LJ, Li SH (2006) Salicylic acid-induced heat or cold tolerance in relation to Ca2+ homeostasis and antioxidant systems in young grape plants. Plant Sci 170(4):685–694.

    CAS  Article  Google Scholar 

  54. Xue X, Liu A, Hua X (2009) Proline accumulation and transcriptional regulation of proline biosynthesis and degradation in Brassica napus. BMB Rep 42:28–34. https://doi.org/10.5483/bmbrep.2009.42.1.028

    CAS  Article  Google Scholar 

  55. Yamasaki S, Dillenburg LR (1999) Measurements of leaf relative water content in Araucaria angustifolia. R Bras Fisiol Veg 11(2):69–75

    Google Scholar 

Download references

Acknowledgements

This study was supported by two research grants at Lorestan University (FPN: B.5107-1397-02-30), Khoramabad, Iran, and Shahid Chamran University, Ahvaz (AG1397 Grant Faculty of Agriculture), Iran.

Author information

Affiliations

Authors

Corresponding author

Correspondence to S. Mousavi-Fard.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Editorial responsibility: Mohamed F. Yassin.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Safari, M., Mousavi-Fard, S., Rezaei Nejad, A. et al. Exogenous salicylic acid positively affects morpho-physiological and molecular responses of Impatiens walleriana plants grown under drought stress. Int. J. Environ. Sci. Technol. (2021). https://doi.org/10.1007/s13762-020-03092-2

Download citation

Keywords

  • Drought stress
  • Impatiens walleriana
  • P5CR: δ1-pyrroline-5-carboxylate reductase gene
  • P5CS: δ1-pyrroline-5-carboxylate synthetase gene
  • Salicylic acid